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Contents lists available at ScienceDirect

Auris Nasus Larynx

journal homepage: www.elsevier.com/locate/anl

Effects of nutritional status and cognitive ability on olfactory function

in geriatric patients
Sung-Yong Jin a,1, Hye Seon Jeong b,1, Jin Woo Lee a, Ki Ryun Kwon a,
Ki-Sang Rha a,c, Yong Min Kim a,c,*
a
b
c

Department of Otorhinolaryngology-Head and Neck Surgery, Chungnam National University School of Medicine, Daejeon, Republic of Korea
Department of Neurology, Chungnam National University School of Medicine, Daejeon, Republic of Korea
Research Institute for Medical Science, Chungnam National University School of Medicine, Daejeon, Republic of Korea

A R T I C L E I N F O

A B S T R A C T

Article history:
Received 22 January 2015
Accepted 29 June 2015
Available online xxx

Objective: The aim of this study was to investigate the prevalence of olfactory dysfunction and evaluate
the relationship between olfactory function and nutritional status, comorbidity, and the results of a
neurocognitive test in geriatric patients who do not suffer from neurodegenerative disease.
Materials and methods: A total of 45 patients who visited the Geriatric Health Center of Chungnam
National University Hospital were enrolled in this study. Olfactory function was assessed using a Korean
Version of Snifn Stick Test II. Cognitive status of all participants was assessed with the MMSE-K (Korean
version of the Mini-Mental State Examination). Nutritional status was assessed with body mass index,
Mini-Nutritional Assessment (MNA), and serum total protein and albumin.
Results: A total of 45 participants were enrolled in this study. Of these subjects, 28 were men and
17 were women, with a mean age of 71.7  5.16 years. Nine (20%) were normosmia, 13 (28.9%) were
hyposmia, and 23 (51.1%) were anosmia. Thirty-six patients (80%) suffered from olfactory dysfunction
(anosmia or hyposmia). MMSE score showed signicant correlation with MNA score. There were signicant
negative correlations between age and total TDI (threshold, discrimination, and identication) score,
discrimination score, identication score, and MMSE score. MMSE score showed signicant correlation with
discrimination score and identication score. However, MNA score did not show any signicant correlation
with olfactory function test results.
Conclusion: Although olfactory function was not inuenced by nutritional status, abilities of
discrimination and identication of odors were associated with cognitive function in geriatric patients.
2015 Elsevier Ireland Ltd. All rights reserved.

Keywords:
Olfaction
Odor identication
Nutrition
Aging
Cognitive impairment
Malnutrition
Smell disorder

1. Introduction
Olfactory dysfunction may be associated with failure to
recognize danger and may accompany social, psychological, and
nutritional problems, as well as decrease quality of life [1]. It has
been known that the overall prevalence of olfactory dysfunction is
estimated around 5% and that the prevalence increases exponentially with age [1,2].
Age-related olfactory loss (presbyosmia) affects critical functions, such as nutrition, immunity, mood, behavior, and sexuality
[3,4], and has been known to be related to high risk of mortality

* Corresponding author at: Department of Otolaryngology-Head and Neck

Surgery, Chungnam National University Hospital, 282 Munhwa-ro, Jung-gu,
Daejeon 301-721, Republic of Korea. Tel.: +82 42 280 7696; fax: +82 42 253 4059.
E-mail address: entkym@cnu.ac.kr (Y.M. Kim).
1
These authors contributed equally to the completion of this article.

[5]. Furthermore, the relationship between olfaction and mortality

may be largely mediated by cognitive impairment [5].
Nutrition is known to be an important element of health and
affects the aging process in the geriatric population [6]. The decline
in sense of smell inhibits avor perception and inuences food
intake in older people and can inuence the type of food eaten.
Indeed, it has been shown that olfaction loss (hyposmia) is
associated with reduced interest in and intake of food [7]. Furthermore, the prevalence of malnutrition is increasing in the geriatric
population and its association with olfactory dysfunction alone or
in combination with taste loss has been demonstrated [8].
Although olfactory function is a very important element in
nutritional status and there is an increasing evidence of a
relationship between malnutrition and olfaction loss in older
adults, little research has been conducted to elucidate this issue.
The aim of this study was to investigate the prevalence of olfactory
dysfunction and to evaluate the relationship between olfactory

http://dx.doi.org/10.1016/j.anl.2015.06.009
0385-8146/ 2015 Elsevier Ireland Ltd. All rights reserved.

Please cite this article in press as: Jin S-Y, et al. Effects of nutritional status and cognitive ability on olfactory function in geriatric
patients. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2015.06.009

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function and nutritional status, comorbidity, and the results of a

neurocognitive test in Korean geriatric patients who do not suffer
from neurodegenerative disease.

and 25 to 48 as normosmia. The criteria used were based on

previous work [9].
2.3. Assessment of functional status and cognitive function

2. Materials and methods

2.1. Patients
A total of 45 patients who visited the Geriatric Health Center of
Chungnam National University Hospital between August 2013 and
March 2014 were enrolled in this study. The population did not
include hospitalized patients, but included only those from an outpatient clinic, specically from the Geriatric Health Center. Most
patients visited this center to evaluate mild headache or cognitive
impairments, and all patients undertook a brain MRI to exclude
organic brain disease. Endoscopic examination of the nasal cavity
was conducted to exclude sinonasal inammation, such as
rhinosinusitis, nasal polyps, or sinonasal tumors, and obstructive
lesions of the olfactory clefts. Additional information was obtained
from brain MRI or plain radiography of the paranasal sinuses to
exclude sinonasal diseases. Exclusion criteria were age less than
65 years; withdrawal of informed consent; diagnosis of Parkinsons, Alzheimer diseases, or other organic brain disease;
moderate or severe cognitive impairment dened as a Mini
Mental State Examination (MMSE) score of less than 20; sinonasal
abnormalities, such as severe nasal septal deviation, rhinosinusitis,
nasal polyposis, sinonasal tumors, or severe allergic rhinitis; and
smoking within the preceding year.
Patient characteristics are included in Table 1. Informed
consent was obtained from each patient before enrollment in
the study. The study was approved by the Institutional Review
Board of the Chungnam National University Hospital.

To evaluate self-caring capacity, Barthel Index was used.

Barthel Index consists of 10 items that measure a persons daily
function, specically the activities of daily living and mobility. The
items include feeding, moving from a wheelchair to bed and
returning, grooming, transferring to and from the toilet, bathing,
walking on a level surface, going up and down stairs, dressing, and
continence of bowels and bladder. Barthel Index is scored from 0 to
100, with 0 points indicating complete care dependency. Cognitive
status of all participants was assessed with the MMSE-K (Korean
version of the Mini-Mental State Examination). The MMSE
contains 19 items and the maximum score is 30 points (10 points
for orientation, 6 for verbal memory, 5 for concentration and
calculation, 5 for language, 3 for praxis, and 1 for visuospatial
construction) [11]. A score of more than 25 points indicates a
normal cognitive status.
2.4. Determination of nutritional status
Blood sampling was performed to measure serum total protein
and albumin levels in each patient. Nutritional status was assessed
with BMI (kg/m2) and Mini-Nutritional Assessment (MNA). The
MNA consists of 18 items including anthropometric measurements
and questions on weight loss within the preceding 3 months,
mobility, food intake, and self-perception of the patient. It is a
validated instrument to screen for malnutrition in older patients
[6,12]. Participants were divided into 3 groups according to
nutritional status: malnutrition (a score of less than 17), risk of
malnutrition (a score of between 17 and 23.5), and well-nourished
patients (a score of over 24 points) [12,13].

2.2. Olfactory function test

2.5. Statistical analysis
Olfactory function was assessed using a validated test, the
Korean version of Snifn Stick Test II (KVSS II, Kwang Woo, Seoul,
Korea) [9]. It consists of 3 different subtest, including a threshold
(T), discrimination (D), and identication (I) test. The tests were
performed in the same way as the Snifn Stick test and previous
work [9,10]. The threshold was dened as the concentration at
which n-butanol (highest concentration 4%, 1:2 serial dilutions to
16 steps) was correctly identied four times in a row. For the
discrimination test, triplets of odorants (two were identical, one
different) were presented and subjects were asked to choose the
odd odorant. The identication test involved 16 odors familiar to
Koreans. The sums of the three tests were presented as a
Threshold-Discrimination-Identication (TDI) score. Total (TDI)
scores of 0 to 20 were dened as anosmia, 21 to 24 as hyposmia,

All statistical analyses were performed using GraphPad Prism 5

(GraphPad, Inc, San Diego, CA, USA). Paired or unpaired Student ttest, MannWhitney U-test, and Spearman correlation tests were
applied with signicance levels set at p < .05.
3. Results
3.1. Patient characteristics
A total of 45 participants were enrolled in this study. Of these
subjects, 28 were men and 17 were women, with a mean age of
71.7  5.16 years (range, 6589). Nine (20%) were classied as
normosmia, 13 (28.9%) were hyposmia, and 23 (51.1%) were anosmia.

Table 1
Patients characteristics.

Age
Male (No.)
Female (No.)
BMI
Total protein
Albumin
KVSSII score
MNA
MMSE
No. of comorbid disease
Barthel Index

Total (n = 45) (mean  SD)

Normosmia (n = 9)

Hyposmia (n = 13)

Anosmia (n = 23)

p-value

71.7  5.16
28
17
24.0  3.2
6.84  0.62
4.07  0.39
20.0  5.7
23.6  2.9
26.4  2.5
3.2  1.4
100

69.3  4.2
5
4
23.3  2.5
7.1  0.75
4.09  0.54
28.3  3.2
22.6  3.1
27.7  2.0
3.1  1.4
100

70.2  4.9
10
3
24.4  3.1
6.78  0.54
4.02  0.32
22.0  1.1
24.9  2.7
26.6  2.7
3.6  1.7
100

73.4  5.0
13
10
24.0  3.5
6.77  0.61
4.08  0.37
15.7  3.3
23.3  2.9
25.9  2.4
2.9  1.1
100

.643
.431
.464
.149
.485
.000
.473
.738
.439

BMI, body mass index; KVSSII, Korean version of Snifn Stick Test II; MNA, Mini-Nutritional Assessment; MMSE, Mini-Mental State Examination.

Please cite this article in press as: Jin S-Y, et al. Effects of nutritional status and cognitive ability on olfactory function in geriatric
patients. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2015.06.009

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Fig. 1. Correlations among the olfactory function test and between Mini-Nutritional Assessment (MNA) and Mini-Mental State Examination (MMSE) scores. There were
signicant correlations between TDI (total) score and threshold (A), discrimination (B), or identication (C) score in this study. In addition, MMSE score showed signicant
correlation with MNA score (D). *a, p < .0001 and b-Coefcient = 0.722 (A), 0.675 (B), 0.798 (C); *b, p = .016 and b-Coefcient = 0.356 (D).

Thirty-six patients (80%) suffered from olfactory dysfunction (anosmia or hyposmia). Barthel Index of all subjects was 100 points, and
mean BMI, KVSS II, MNA, and MMSE scores were 24.0  3.2,
20.0  5.7, 23.6  2.9, and 26.4  2.5, respectively (Table 1).
Comorbid diseases were also analyzed, and the most common
comorbid disease was hypertension (n = 27), followed by hyperlipidemia (n = 14), diabetes mellitus (DM, n = 8), urology disease
(n = 8), peripheral vascular disease (n = 6), cardiovascular disease
(n = 5), skeletal disease (n = 4), and gastrointestinal disease (n = 2).
There was no signicant correlation between olfactory function
test and number of comorbid diseases. However, number of
comorbid disease showed signicant correlation with BMI
(p = .0373).

correlations between age and TDI (Fig. 2A, p = .0380), discrimination (Fig. 2C, p = .0054), identication (Fig. 2D, p = .0438), and
MMSE scores (Fig. 2E, p = .0009). Threshold and MNA scores did not
show any signicant correlation with age (Fig. 2B and 2F).

3.2. Correlations of olfactory function test, MNA, and MMSE

3.4. Analysis of factors inuencing body mass index

There were signicant correlations between TDI (total) score

and threshold (Fig. 1A, p < .0001), discrimination (Fig. 1B,
p < .0001), or identication score (Fig. 1C, p < .0001) in this study.
In addition, MMSE score showed signicant correlation with
MNA score (Fig. 1D, p = .0116). There were signicant negative

In a linear regression analysis with BMI as dependent variable,

age, number of disease, MMSE, MNA, and threshold score of KVSS II
test were factors with signicant inuence (Table 4). However, BMI
was affected by total score, discrimination score, or identication
score.

3.3. Analysis of factors inuencing cognitive function and nutritional

status
MMSE score was affected by discrimination and identication
scores (Table 2). However, MNA score did not show any signicant
correlation with discrimination and identication scores, though
there was a signicant negative correlation with threshold score
(Table 3).

Table 2
Linear regression analysis of factors inuencing cognitive function.
Mini-Mental State Examination

b-Coefcient
Age
Gender
No. of disease
MNA
KVSSII score
Threshold
Discrimination
Identication

0.234
0.197
0.122
0.356
0.226
0.095
0.340
0.280

SE

p-value

0.066
0.757
0.275
0.121
0.064
0.139
0.157
0.130

.001
.194
.426
.016
.135
.535
.022
.037

OR (95% CI)
0.234
0.998
0.221
0.301
0.098
0.087
0.371
0.249

[ 0.367 to 0.102]
[ 2.524 to 0.529]
[ 0.776 to 0.334]
[0.058 to 0.545]
[ 0.032 to 0.228]
[ 0.366 to 0.193]
[0.055 to 0.687]
[ 0.014 to 0.511]

MNA, Mini-Nutritional Assessment; KVSSII, Korean version of Snifn Stick Test II.

Please cite this article in press as: Jin S-Y, et al. Effects of nutritional status and cognitive ability on olfactory function in geriatric
patients. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2015.06.009

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Fig. 2. Correlations between age and olfactory function test, Mini-Mental State Examination (MMSE) or Mini-Nutritional Assessment (MNA) scores. There were signicant
negative correlations between age and TDI (A), discrimination (C), identication (D), and MMSE scores (E). *a, p = .0380 and b-Coefcient = 0.312; *b, p = .0054 and bCoefcient = 0.408; *c, p = .0438 and b-Coefcient = 0.302; *d, p = .0009 and b-Coefcient = 0.479.
Table 3
Linear regression analysis of factors inuencing nutritional status.
Mini-Nutritional Assessment

b-Coefcient
Age
Gender
No. of disease
MMSE
KVSSII score
Threshold
Discrimination
Identication

0.282
0.430
0.018
0.356
0.029
0.298
0.186
0.080

SE

p-value

0.085
0.823
0.328
0.168
0.078
0.157
0.193
0.159

.061
.003
.906
.016
.852
.046
.221
.600

OR (95% CI)
0.163
2.571
0.039
0.420
0.015
0.322
0.240
0.084

[ 0.334 to 0.008]
[ 4.232 to 0.911]
[ 0.700 to 0.622]
[0.081 to 0.760]
[ 0.172 to 0.143]
[ 0.638 to 0.005]
[ 0.150 to 0.630]
[ 0.237 to 0.406]

MMSE, Mini-Mental State Examination; KVSSII, Korean version of Snifn Stick Test II.

Serum total protein and albumin levels were measured in each

patient; however, they did not show any signicant correlations
with BMI, MNA, or TDI score in this study (Fig. 3).
4. Discussion
This study was conducted to investigate the prevalence of
olfactory dysfunction and the relationship between an olfactory
function test and nutritional status, comorbidity, and the results of
a neurocognitive test in Korean geriatric patients. The prevalence
of olfactory dysfunction (anosmia or hyposmia) was 24.570.2% in

previous studies, and olfactory performance was found to decrease

with age [2,12,14]. Prevalence of olfactory dysfunction in our study
was 80% (36 out of 45), and olfactory functioning also negatively
correlated with increasing age. The higher prevalence of olfactory
dysfunction in our patients was probably due to the fact that they
were not from the general population. They suffered from various
diseases, such as hypertension, DM, hyperlipidemia, and peripheral vascular disease, and were consequently seeking therapy for
these diseases at the Geriatric Health Center.
It has been shown that men tend to have a poorer olfactory
function than women, and the odds of men developing olfactory

Please cite this article in press as: Jin S-Y, et al. Effects of nutritional status and cognitive ability on olfactory function in geriatric
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Table 4
Linear regression analysis of factors inuencing body mass index.
Body Mass Index

b-Coefcient
Age
Gender
No. of disease
MMSE
MNA
KVSSII score
Threshold
Discrimination
Identication

0.457
0.095
0.311
0.327
0.330
0.113
0.359
0.116
0.024

SE

p-value

0.085
0.986
0.338
0.185
0.156
0.084
0.167
0.212
0.174

.002
.535
.037
.028
.027
.460
.015
.449
.875

OR (95% CI)
0.287
0.617
0.727
0.420
0.358
0.063
0.421
0.162
0.027

[ 0.459 to 0.115]
[ 1.371 to 2.605]
[0.045 to 1.409]
[0.047 to 0.792]
[0.043 to 0.673]
[ 0.233 to 0.107]
[ 0.757 to 0.085]
[ 0.266 to 0.590]
[ 0.323 to 0.378]

MMSE, Mini-Mental State Examination; MNA, Mini-Nutritional Assessment; KVSSII, Korean version of Snifn Stick Test II.

Fig. 3. Correlations between and serum total protein or albumin levels and body mass index (BMI, A and B), Mini-Nutritional Assessment (MNA) scores (C and D), and TDI
(total) score of olfactory function test and b-Coefcient = 0.170 (A), 0.192 (B), 0.147 (C), 0.100 (D), 0.094 (E), and 0.017 (F).

dysfunction were more than double compared with women

[2,14,15]. In the present study, men also showed a higher prevalence
of olfactory impairment (n = 23, 51%) than women (n = 13, 29%) even
though our patient sample population was smaller.
Total score of KVSS II showed very strong correlations with its
threshold, discrimination, and identication tests in the present
study (Fig. 1). In spite of the strong correlation among the tests,
each test demonstrates unique characteristics when it is conducted
separately and may contribute to localize underlying pathology. If
only the ability of discrimination or identication is affected,

impairment of the central nervous system could be suspected,

while isolated shifting of the olfactory threshold tends to indicate
peripheral damage [16,17]. In the present study, MMSE, which
assessed cognitive function of the geriatric patients, showed
signicant positive correlation with discrimination and identication scores. As patients with severe cognitive dysfunction and
Parkinsons disease are known to have olfactory dysfunction [18],
and olfactory dysfunction could be an early symptom of
neurodegenerative diseases such as Parkinsons disease and
Alzheimer dementia [19], we excluded these patients from our

Please cite this article in press as: Jin S-Y, et al. Effects of nutritional status and cognitive ability on olfactory function in geriatric
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study. Despite the exclusion of these patients, decreasing cognitive

function scores correlated with decreasing discrimination and
identication scores. Aging is known to be associated with a
general decline in cognitive abilities [20], which would explain the
decreasing discrimination and identication scores in this study.
Nutrition is an important element of health in the geriatric
population, and some studies have reported that it can be
inuenced by diminished senses of smell and taste [21,22].
Whereas, other studies have reported that olfactory dysfunction
was not associated with nutritional status [12,15,23]. In our study,
nutritional status was evaluated by MNA score, BMI, and serum
total protein and albumin level. BMI showed signicant correlation
with MNA score. However, serum protein or albumin level did not
show any signicant correlation with BMI or MNA score. Serum
proteins synthesized by the liver have been used as markers of
nutrition. Serum albumin is the most commonly used marker since
it can predict mortality in older people [6]. However, albumin can
be affected by not only nutritional state but also by other factors,
including inammation and infection. This limits their usefulness,
especially in acutely unwell patients [6]. Measurement of BMI and
MNA score, however, may be suitable for evaluating nutritional
status. Nonetheless, the parameters that we used did not show any
signicant correlation with olfactory function test results except
threshold score and BMI (Table 4). The threshold score of the KVSS
II test showed signicant negative correlation with BMI, and this
result could be explained by the fact that older patients with
decreasing olfactory function have compensatory strategies that
may have already developed such as preference for foods with
enhanced primary taste qualities (e.g., salty or sugary)
[12,24]. These compensatory strategies could result in increased
food intake and weight gain in the patients with olfactory
dysfunction.
In addition, pathologic changes during aging, such as chronic
disease and psychological illness, may play roles as important
etiologies of malnutrition in older people. We investigated
comorbid disease in our patients and analyzed the relationship
with olfactory function test results and nutritional assessment. The
number of comorbid diseases showed signicant positive correlation with BMI. Measurement of BMI in geriatric patients has certain
limits such as height change due to vertebral collapse and loss of
muscle tone. In these cases, measurement of certain body
segments, such as leg, arm and arm span, could be reliable to
obtain height [6,25]. In addition, there could be confounding
factors such as ascites and edema to warrant avoiding use of BMI as
a surrogate marker of nutrition [6].
In the present study, cognitive function test (MMSE score)
showed signicant correlation with BMI and MNA score. These
results indicated that cognitive function of geriatric patients could be
associated with nutritional state. However, nutritional status did not
impact on olfactory function in these patients, and olfactory decits
in this geriatric population with normal functionality and performance did not have any inuence on impaired nutritional status.
Apart from teratogenic and pathological effects of zinc
deciency, such as the occurrence of skin lesions, anorexia, growth
retardation, depressed wound healing, altered immune function,
and impaired night vision, alterations in taste and smell acuity in
animal models and human patients suffering from zinc deciency
have been observed. However, it is known that severe zinc
deciency is rare and difcult to substantiate. Unfortunately, we
did not routinely examine serum zinc levels in this study. Because
we included patients from an outpatient clinic with high
functioning and performance and their nutritional status was
relatively good, there was no possibility that zinc deciency
patients were included in this study.
Although olfactory function was not inuenced by nutritional
status, the abilities of discrimination and identication of odors

were associated with cognitive function in geriatric patients. As the

study participants were higher functioning older adults who
visited our Geriatric Health Center, they were not representative of
the general elder population. Therefore, further studies of
participants with high risk of nutritional deciency and larger
sample populations will be needed in the future.

Financial disclosure
This work (research) was supported by Chungnam National
University Hospital Research Fund 2013.

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Please cite this article in press as: Jin S-Y, et al. Effects of nutritional status and cognitive ability on olfactory function in geriatric
patients. Auris Nasus Larynx (2015), http://dx.doi.org/10.1016/j.anl.2015.06.009